Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis
Abstract
Alternation between morphologically distinct haploid and diploid life forms is a defining feature of most plant and algal life cycles, yet the underlying molecular mechanisms that govern these transitions remain unclear. Here, we explore the dynamic relationship between chromatin accessibility and epigenetic modifications during life form transitions in Arabidopsis. The diploid-to-haploid life form transition is governed by the loss of H3K9me2 and DNA demethylation of transposon-associated cis-regulatory elements. This event is associated with dramatic changes in chromatin accessibility and transcriptional reprogramming. In contrast, the global loss of H3K27me3 in the haploid form shapes a chromatin accessibility landscape that is poised to re-initiate the transition back to diploid life after fertilization. Hence, distinct epigenetic reprogramming events rewire transcription through major reorganization of the regulatory epigenome to guide the alternation of generations in flowering plants.
Data availability
Deep-sequencing data that support the findings of this study have been deposited in the Gene Expression Omnibus (GEO) under accession code GSE155369. Re-analysis of previously published DNA methylomes from dme-2/+ pollen (Ibarra et al., 2012), and siRNAs from leaves (Papareddy et al., 2020) and pollen (Borges et al., 2018; Slotkin et al., 2009) were deposited in the GEO under accession code GSE155369.
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Epigenetic reprogramming rewires transcription during the alternation of generations in ArabidopsisNCBI Gene Expression Omnibus, GSE155369.
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Active DNA demethylation in plant companion cells reinforces transposon methylation in gametesNCBI Gene Expression Omnibus, GSE38935.
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Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatinNCBI Gene Expression Omnibus, GSE120669.
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Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in ArabidopsisNCBI Gene Expression Omnibus, GSE106117.
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Epigenetic reprogramming and small RNA silencing of transposable elements in pollenNCBI Gene Expression Omnibus, GSE61028.
Article and author information
Author details
Funding
Austrian Science Fund (P26887)
- Frédéric Berger
Austrian Science Fund (I 4258)
- Frédéric Berger
Austrian Science Fund (I2163-B16)
- Frédéric Berger
Austrian Science Fund (M1818)
- Michael Borg
European Commission (ERC 637888)
- Michael D Nodine
Biotechnology and Biological Sciences Research Council (BB/I011269/1)
- David Twell
Biotechnology and Biological Sciences Research Council (BB/N005090)
- David Twell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Richard Amasino, University of Wisconsin Madison, United States
Version history
- Received: August 7, 2020
- Accepted: January 25, 2021
- Accepted Manuscript published: January 25, 2021 (version 1)
- Version of Record published: March 1, 2021 (version 2)
Copyright
© 2021, Borg et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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